Multi-trait association mapping for phosphorous efficiency reveals flexible root architectures in sorghum

Background On tropical regions, phosphorus (P) fixation onto aluminum and iron oxides in soil clays restricts P diffusion from the soil to the root surface, limiting crop yields. While increased root surface area favors P uptake under low-P availability, the relationship between the three-dimensional arrangement of the root system and P efficiency remains elusive. Here, we simultaneously assessed allelic effects of loci associated with a variety of root and P efficiency traits, in addition to grain yield under low-P availability, using multi-trait genome-wide association. We also set out to establish the relationship between root architectural traits assessed in hydroponics and in a low-P soil. Our goal was to better understand the influence of root morphology and architecture in sorghum performance under low-P availability. Result In general, the same alleles of associated SNPs increased root and P efficiency traits including grain yield in a low-P soil. We found that sorghum P efficiency relies on pleiotropic loci affecting root traits, which enhance grain yield under low-P availability. Root systems with enhanced surface area stemming from lateral root proliferation mostly up to 40 cm soil depth are important for sorghum adaptation to low-P soils, indicating that differences in root morphology leading to enhanced P uptake occur exactly in the soil layer where P is found at the highest concentration. Conclusion Integrated QTLs detected in different mapping populations now provide a comprehensive molecular genetic framework for P efficiency studies in sorghum. This indicated extensive conservation of P efficiency QTL across populations and emphasized the terminal portion of chromosome 3 as an important region for P efficiency in sorghum. Increases in root surface area via enhancement of lateral root development is a relevant trait for sorghum low-P soil adaptation, impacting the overall architecture of the sorghum root system. In turn, particularly concerning the critical trait for water and nutrient uptake, root surface area, root system development in deeper soil layers does not occur at the expense of shallow rooting, which may be a key reason leading to the distinctive sorghum adaptation to tropical soils with multiple abiotic stresses including low P availability and drought. Supplementary Information The online version contains supplementary material available at 10.1186/s12870-024-05183-5.

).The SNP designations shown in (B) consist of the letter "S" (SNP) followed by the respective chromosome number and physical position in bp.Estimated SNP effects (blue dots) and 95% confidence intervals (vertical line) are shown.
The horizontal red dashed line at zero indicates there was no statistically significant difference for the effect of the two homozygous classes at each SNP locus.Hence, the confidence intervals for significant SNPs do not overlap with the dashed line.The effect signs, either positive or negative, indicate the origin of the allele that increases phenotypic expression of a given trait (i.e.favorable allele).SNPs with positive effect signs have the minor allele (allele with a frequency < 0.5) as favorable, whereas negative signs indicate that the alleles with frequency > 0.5 (major allele) increase the phenotype.All traits were standardized before MT-GWAS to have zero means and total phenotypic variance equal to 1.  S3).The SNP designations shown in (B) consist of the letter "S" (SNP) followed by the respective chromosome number and physical position in bp.Estimated SNP effects (blue dots) and 95% confidence intervals (vertical line) are shown.
The horizontal red dashed line at zero indicates there was no statistically significant difference for the effect of the two homozygous classes at each SNP locus.Hence, the confidence intervals for significant SNPs do not overlap with the dashed line.The effect signs, either positive or negative, indicate the origin of the allele that increases phenotypic expression of a given trait (i.e.favorable allele).SNPs with positive effect signs have the minor allele (allele with a frequency < 0.5) as favorable, whereas negative signs indicate that the alleles with frequency > 0.5 (major allele) increase the phenotype.All traits were standardized before MT-GWAS to have zero means and total phenotypic variance equal to 1.  S3).The SNP designations shown in (C) and (D) consist of the letter "S" (SNP) followed by the respective chromosome number and physical position in bp.Estimated SNP effects (blue dots) and 95% confidence intervals (vertical line) are shown.The horizontal red dashed line at zero indicates there was no statistically significant difference for the effect of the two homozygous classes at each SNP locus.Hence, the confidence intervals for significant SNPs do not overlap with the dashed line.The effect signs, either positive or negative, indicate the origin of the allele that increases phenotypic expression of a given trait (i.e.favorable allele).SNPs with positive effect signs have the minor allele (allele with a frequency < 0.5) as favorable, whereas negative signs indicate that the alleles with frequency > 0.5 (major allele) increase the phenotype.All traits were standardized before MT-GWAS to have zero means and total phenotypic variance equal to 1.  S3).The SNP designations shown in (C) and (D) consist of the letter "S" (SNP) followed by the respective chromosome number and physical position in bp.Estimated SNP effects (blue dots) and 95% confidence intervals (vertical line) are shown.The horizontal red dashed line at zero indicates there was no statistically significant difference for the effect of the two homozygous classes at each SNP locus.Hence, the confidence intervals for significant SNPs do not overlap with the dashed line.The effect signs, either positive or negative, indicate the origin of the allele that increases phenotypic expression of a given trait (i.e.favorable allele).SNPs with positive effect signs have the minor allele (allele with a frequency < 0.5) as favorable, whereas negative signs indicate that the alleles with frequency > 0.5 (major allele) increase the phenotype.All traits were standardized before MT-GWAS to have zero means and total phenotypic variance equal to 1.

Fig. S2
Fig. S2 Estimated effects for additional SNPs that were significantly associated with multiple traits by MT-GWAS.The physical coordinates (in base pairs, bp, based on the sorghum genome version 2.1), next to each associated SNP are shown for SNPs on chromosomes 3 (A).Associated SNPs (green) and SNPs within a physical window of 150 Kb (in blue, depicting the estimated extent of LD in sorghum, Morris et al. [29]) around the associated SNPs are highlighted.The red dashed line depicts the -log10(p) = 4.0 threshold.Estimated effects for SNPs on chromosomes 3 with maximum -log10(p) by MT-GWAS are shown in (B) (explained phenotypic variances for each SNP are in TableS3).The SNP designations shown in (B) consist

Fig. S3
Fig. S3 Estimated effects for additional SNPs that were significantly associated with multiple traits by MT-GWAS.The physical coordinates (in base pairs, bp, based on the sorghum genome version 2.1), next to each associated SNP are shown for SNPs on chromosomes 5 (A).Associated SNPs (green) and SNPs within a physical window of 150 Kb (in blue, depicting the estimated extent of LD in sorghum, Morris et al., [29]) around the associated SNPs are highlighted.The red dashed line depicts the -log10(p) = 4.0 threshold.Estimated effects for SNPs on chromosomes 5 with maximum -log10(p) by MT-GWAS are shown in (B) (explained phenotypic variances for each SNP are in TableS3).The SNP designations shown in (B) consist

Fig. S4
Fig. S4 Estimated effects for SNPs that were significantly associated with multiple traits by MT-GWAS.The physical coordinates (in base pairs, bp, based on the sorghum genome version 2.1), next to each associated SNP are shown for SNPs on chromosomes 6 (A) and 7 (B).Associated SNPs (green) and SNPs within a physical window of 150 Kb (in blue, depicting the estimated extent of LD in sorghum, Morris et al. [29]) around the associated SNPs are highlighted.The red dashed line depicts the -log10(p) = 4.0 threshold.Estimated effects for

Fig. S5
Fig. S5 Estimated effects for SNPs that were significantly associated with multiple traits by MT-GWAS.The physical coordinates (in base pairs, bp, based on the sorghum genome version 2.1), next to each associated SNP are shown for SNPs on chromosomes 9 (A) and 10 (B).Associated SNPs (green) and SNPs within a physical window of 150 Kb (in blue, depicting the estimated extent of LD in sorghum, Morris et al., [29]) around the associated SNPs are highlighted.The red dashed line depicts the -log10(p) = 4.0 threshold.Estimated effects for SNPs on chromosomes 9 and 10 with maximum -log10(p) by MT-GWAS are shown in (C) and (D), respectively (explained phenotypic variances for each SNP are in TableS3).The SNP